INF2 promotes the formation of detyrosinated microtubules necessary for centrosome reorientation in T cells

  1. Andrés-Delgado, Laura 2
  2. Antón, Olga M. 2
  3. Bartolini, Francesca 1
  4. Ruiz-Sáenz, Ana 2
  5. Correas, Isabel 2
  6. Gundersen, Gregg G. 1
  7. Alonso, Miguel A. 2
  1. 1 Department of Pathology and Cell Biology, Columbia University, New York, NY 10032 2
  2. 2 Centro de Biología Molecular “Severo Ochoa,” Consejo Superior de Investigaciones Científicas/Universidad Autónoma de Madrid, Cantoblanco, 28049 Madrid, Spain 1
Revista:
Journal of Cell Biology

ISSN: 1540-8140 0021-9525

Año de publicación: 2012

Volumen: 198

Número: 6

Páginas: 1025-1037

Tipo: Artículo

DOI: 10.1083/JCB.201202137 GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: Journal of Cell Biology

Resumen

T cell antigen receptor–proximal signaling components, Rho-family GTPases, and formin proteins DIA1 and FMNL1 have been implicated in centrosome reorientation to the immunological synapse of T lymphocytes. However, the role of these molecules in the reorientation process is not yet defined. Here we find that a subset of microtubules became rapidly stabilized and that their α-tubulin subunit posttranslationally detyrosinated after engagement of the T cell receptor. Formation of stabilized, detyrosinated microtubules required the formin INF2, which was also found to be essential for centrosome reorientation, but it occurred independently of T cell receptor–induced massive tyrosine phosphorylation. The FH2 domain, which was mapped as the INF2 region involved in centrosome repositioning, was able to mediate the formation of stable, detyrosinated microtubules and to restore centrosome translocation in DIA1-, FMNL1-, Rac1-, and Cdc42-deficient cells. Further experiments indicated that microtubule stabilization was required for centrosome polarization. Our work identifies INF2 and stable, detyrosinated microtubules as central players in centrosome reorientation in T cells.

Referencias bibliográficas

  • Andrés-Delgado, (2010), Blood., 116, pp. 5919, 10.1182/blood-2010-08-300665
  • Baratt, (2008), PLoS ONE., 3, pp. e3861, 10.1371/journal.pone.0003861
  • Bartolini, (2010), Biochim. Biophys. Acta., 1803, pp. 164, 10.1016/j.bbamcr.2009.07.006
  • Bartolini, (2008), J. Cell Biol., 181, pp. 523, 10.1083/jcb.200709029
  • Billadeau, (2007), Nat. Rev. Immunol., 7, pp. 131, 10.1038/nri2021
  • Boyer, (2011), N. Engl. J. Med., 365, pp. 2377, 10.1056/NEJMoa1109122
  • Brown, (2010), Nat. Genet., 42, pp. 72, 10.1038/ng.505
  • Butler, (2009), Curr. Biol., 19, pp. 1886, 10.1016/j.cub.2009.10.029
  • Chhabra, (2006), J. Biol. Chem., 281, pp. 26754, 10.1074/jbc.M604666200
  • Combs, (2006), Proc. Natl. Acad. Sci. USA., 103, pp. 14883, 10.1073/pnas.0600914103
  • Cook, (1998), J. Cell Biol., 141, pp. 175, 10.1083/jcb.141.1.175
  • Derry, (1995), Biochemistry., 34, pp. 2203, 10.1021/bi00007a014
  • Dunn, (2008), J. Cell Sci., 121, pp. 1085, 10.1242/jcs.026492
  • Erck, (2005), Proc. Natl. Acad. Sci. USA., 102, pp. 7853, 10.1073/pnas.0409626102
  • Fooksman, (2010), Annu. Rev. Immunol., 28, pp. 79, 10.1146/annurev-immunol-030409-101308
  • Gaillard, (2011), Mol. Biol. Cell., 22, pp. 4575, 10.1091/mbc.E11-07-0616
  • Galjart, (2010), Curr. Biol., 20, pp. R528, 10.1016/j.cub.2010.05.022
  • Galjart, (2003), Curr. Opin. Cell Biol., 15, pp. 48, 10.1016/S0955-0674(02)00007-8
  • Gil, (2002), Cell., 109, pp. 901, 10.1016/S0092-8674(02)00799-7
  • Gomes, (2005), Cell., 121, pp. 451, 10.1016/j.cell.2005.02.022
  • Gomez, (2007), Immunity., 26, pp. 177, 10.1016/j.immuni.2007.01.008
  • Goode, (2007), Annu. Rev. Biochem., 76, pp. 593, 10.1146/annurev.biochem.75.103004.142647
  • Griffiths, (2010), J. Cell Biol., 189, pp. 399, 10.1083/jcb.201002027
  • Gundersen, (1988), Proc. Natl. Acad. Sci. USA., 85, pp. 5946, 10.1073/pnas.85.16.5946
  • Gundersen, (1984), Cell., 38, pp. 779, 10.1016/0092-8674(84)90273-3
  • Gundersen, (1987), J. Cell Biol., 105, pp. 251, 10.1083/jcb.105.1.251
  • Harris, (2006), J. Biol. Chem., 281, pp. 14383, 10.1074/jbc.M510923200
  • Insall, (2009), Dev. Cell., 17, pp. 310, 10.1016/j.devcel.2009.08.012
  • Knox, (1993), Cell Motil. Cytoskeleton., 24, pp. 129, 10.1002/cm.970240206
  • Konishi, (2009), Nat. Neurosci., 12, pp. 559, 10.1038/nn.2314
  • Kreitzer, (1999), Mol. Biol. Cell., 10, pp. 1105, 10.1091/mbc.10.4.1105
  • Krummel, (2000), Science., 289, pp. 1349, 10.1126/science.289.5483.1349
  • Kuhn, (2002), Immunity., 16, pp. 111, 10.1016/S1074-7613(02)00262-5
  • Kuhné, (2003), J. Immunol., 171, pp. 860, 10.4049/jimmunol.171.2.860
  • Kupfer, (1984), J. Immunol., 133, pp. 2762, 10.4049/jimmunol.133.5.2762
  • Lettau, (2009), Cell Commun. Signal., 7, pp. 1, 10.1186/1478-811X-7-1
  • Ley, (1994), Eur. J. Immunol., 24, pp. 99, 10.1002/eji.1830240116
  • Li, (2008), Nat. Rev. Mol. Cell Biol., 9, pp. 860, 10.1038/nrm2522
  • Lin, (2002), Mol. Biol. Cell., 13, pp. 96, 10.1091/mbc.01-05-0224
  • Lowin-Kropf, (1998), J. Cell Biol., 140, pp. 861, 10.1083/jcb.140.4.861
  • Madrid, (2010), Dev. Cell., 18, pp. 814, 10.1016/j.devcel.2010.04.001
  • Martín-Cófreces, (2008), J. Cell Biol., 182, pp. 951, 10.1083/jcb.200801014
  • Niedergang, (1997), J. Immunol., 159, pp. 1703, 10.4049/jimmunol.159.4.1703
  • Palazzo, (2001), Nat. Cell Biol., 3, pp. 723, 10.1038/35087035
  • Palazzo, (2001), Curr. Biol., 11, pp. 1536, 10.1016/S0960-9822(01)00475-4
  • Palazzo, (2004), Science., 303, pp. 836, 10.1126/science.1091325
  • Peris, (2006), J. Cell Biol., 174, pp. 839, 10.1083/jcb.200512058
  • Peris, (2009), J. Cell Biol., 185, pp. 1159, 10.1083/jcb.200902142
  • Ramabhadran, (2011), Mol. Biol. Cell., 22, pp. 4822, 10.1091/mbc.E11-05-0457
  • Schmoranzer, (2009), Curr. Biol., 19, pp. 1065, 10.1016/j.cub.2009.05.065
  • Sedwick, (1999), J. Immunol., 162, pp. 1367, 10.4049/jimmunol.162.3.1367
  • Serrador, (2004), Immunity., 20, pp. 417, 10.1016/S1074-7613(04)00078-0
  • Smith-Garvin, (2009), Annu. Rev. Immunol., 27, pp. 591, 10.1146/annurev.immunol.021908.132706
  • Stinchcombe, (2007), Annu. Rev. Cell Dev. Biol., 23, pp. 495, 10.1146/annurev.cellbio.23.090506.123521
  • Stinchcombe, (2006), Nature., 443, pp. 462, 10.1038/nature05071
  • Stowers, (1995), Proc. Natl. Acad. Sci. USA., 92, pp. 5027, 10.1073/pnas.92.11.5027
  • Sun, (2011), Proc. Natl. Acad. Sci. USA., 108, pp. 2933, 10.1073/pnas.1017010108
  • Tsun, (2011), J. Cell Biol., 192, pp. 663, 10.1083/jcb.201008140
  • Watanabe, (1997), EMBO J., 16, pp. 3044, 10.1093/emboj/16.11.3044
  • Wen, (2004), Nat. Cell Biol., 6, pp. 820, 10.1038/ncb1160
  • Witte, (2008), J. Cell Biol., 180, pp. 619, 10.1083/jcb.200707042
  • Wloga, (2010), J. Cell Sci., 123, pp. 3447, 10.1242/jcs.063727
  • Xu, (2004), Cell., 116, pp. 711, 10.1016/S0092-8674(04)00210-7
  • Yayoshi-Yamamoto, (2000), Mol. Cell. Biol., 20, pp. 6872, 10.1128/MCB.20.18.6872-6881.2000
  • Zyss, (2011), J. Cell Biol., 195, pp. 781, 10.1083/jcb.201106025